The evolution of fungal substrate specificity in a widespread group of crustose lichens

Lichens exhibit varying degrees of specialization with regard to the surfaces they colonize, ranging from substrate generalists to strict substrate specialists. Though long recognized, the causes and consequences of substrate specialization are poorly known. Using a phylogeny of a 150-200 Mya clade of lichen fungi, we asked whether substrate niche is phylogenetically conserved, which substrates are ancestral, whether specialists arise from generalists or vice versa and how specialization affects speciation/extinction processes. We found strong phylogenetic signal for niche conservatism. Specialists evolved into generalists and back again, but transitions from generalism to specialism were more common than the reverse. Our models suggest that for this group of fungi, 'escape' from specialization for soil, rock and bark occurred, but specialization for wood foreclosed evolution away from that substrate type. In parallel, speciation models showed positive diversification rates for soil and rock dwellers but not other specialists. Patterns in the studied group suggest that fungal substrate specificity is a key determinant of evolutionary trajectory for the entire lichen symbiosis

The Plot Thickens: Haploid and Triploid-Like Thalli, Hybridization, and Biased Mating Type Ratios in Letharia

The study of the reproductive biology of lichen fungal symbionts has been traditionally challenging due to their complex lifestyles. Against the common belief of haploidy, a recent genomic study found a triploid-like signal in Letharia. Here, we infer the genome organization and reproduction in Letharia by analyzing genomic data from a pure culture and from thalli, and performing a PCR survey of the MAT locus in natural populations. We found that the read count variation in the four Letharia specimens, including the pure culture derived from a single sexual spore of L. lupina, is consistent with haploidy. By contrast, the L. lupina read counts from a thallus' metagenome are triploid-like. Characterization of the mating-type locus revealed a conserved heterothallic configuration across the genus, along with auxiliary genes that we identified. We found that the mating-type distributions are balanced in North America for L. vulpina and L. lupina, suggesting widespread sexual reproduction, but highly skewed in Europe for L. vulpina, consistent with predominant asexuality. Taken together, we propose that Letharia fungi are heterothallic and typically haploid, and provide evidence that triploid-like individuals are hybrids between L. lupina and an unknown Letharia lineage, reconciling classic systematic and genetic studies with recent genomic observations

Genome-level analyses resolve an ancient lineage of symbiotic ascomycetes

Ascomycota account for about two-thirds of named fungal species.1 Over 98% of known Ascomycota belong to the Pezizomycotina, including many economically important species as well as diverse pathogens, decomposers, and mutualistic symbionts.2 Our understanding of Pezizomycotina evolution has until now been based on sampling traditionally well-defined taxonomic classes.3,4,5 However, considerable diversity exists in undersampled and uncultured, putatively early-diverging lineages, and the effect of these on evolutionary models has seldom been tested. We obtained genomes from 30 putative early-diverging lineages not included in recent phylogenomic analyses and analyzed these together with 451 genomes covering all available ascomycete genera. We show that 22 of these lineages, collectively representing over 600 species, trace back to a single origin that diverged from the common ancestor of Eurotiomycetes and Lecanoromycetes over 300 million years BP. The new clade, which we recognize as a more broadly defined Lichinomycetes, includes lichen and insect symbionts, endophytes, and putative mycorrhizae and encompasses a range of morphologies so disparate that they have recently been placed in six different taxonomic classes. To test for shared hidden features within this group, we analyzed genome content and compared gene repertoires to related groups in Ascomycota. Regardless of their lifestyle, Lichinomycetes have smaller genomes than most filamentous Ascomycota, with reduced arsenals of carbohydrate-degrading enzymes and secondary metabolite gene clusters. Our expanded genome sample resolves the relationships of numerous “orphan” ascomycetes and establishes the independent evolutionary origins of multiple mutualistic lifestyles within a single, morphologically hyperdiverse clade of fungi

Global phylogeny and taxonomic reassessment of the lichen genus Dendriscosticta (Ascomycota: Peltigerales)

peer reviewedThe genus Dendriscosticta (Ascomycota: Peltigerales) encompasses several distinctive lichen-forming fungal species restricted to the Northern Hemisphere. Most are flagship species of old-growth forests with good air quality. A global phylogeny of the genus based on multilocus sequence data (ITS, RPB1, EF-1α, MCM7), model-based phylogenetic methods, and morphological and chemical assessments, reveals a high level of cryptic speciation often associated with restricted geographical distribution and/or chemical characters. Using sequence-based species delimitation approaches, we circumscribe two main clades referred to as the D. wrightii clade, with five unequivocal species, including D. gelida sp. nov., and the D. praetextata clade, with eight putative species, including D. phyllidiata sp. nov. The absence of recently collected material of D. hookeri comb. nov. from the type locality unfortunately prevents assignment of this epithet to one of the five supported lineages sharing this morphotype. Three new combinations are proposed: D. hookeri, D. insinuans comb. nov. and D. yatabeana comb. nov. Epitypes are designated for D. wrightii and D. yatabeana. Species diversity within the genus increased from four to nine. Our morphological assessment confirmed that Sticta and Dendriscosticta can be readily distinguished by the presence of excipular algae whereas the structure of the lower surface pores is not a reliable diagnostic feature

Data from: Escape from the cryptic species trap: lichen evolution on both sides of a cyanobacterial acquisition event

Large, architecturally complex lichen symbioses arose only a few times in evolution, increasing thallus size by orders of magnitude over those from which they evolved. The innovations that enabled symbiotic assemblages to acquire and maintain large sizes are unknown. We mapped morphometric data against an eight-locus fungal phylogeny across one of the best-sampled thallus size transition events, the origins of the Placopsis lichen symbiosis, and used a phylogenetic comparative framework to explore the role of nitrogen-fixing cyanobacteria in size differences. Thallus thickness increased by >150% and fruiting body core volume increased ninefold on average after acquisition of cyanobacteria. Volume of cyanobacteria-containing structures (cephalodia), once acquired, correlates with thallus thickness in both phylogenetic generalized least squares and phylogenetic generalized linear mixed-effects analyses. Our results suggest that the availability of nitrogen is an important factor in the formation of large thalli. Cyanobacterial symbiosis appears to have enabled lichens to overcome size constraints in oligotrophic environments such as acidic, rain-washed rock surfaces. In the case of the Placopsis fungal symbiont, this has led to an adaptive radiation of more than 60 recognized species from related crustose members of the genus Trapelia. Our data suggest that precyanobacterial symbiotic lineages were constrained to forming a narrow range of phenotypes, so-called cryptic species, leading systematists until now to recognize only six of the 13 species clusters we identified in Trapelia

StarBEAST_MCC_run1_Schneider_et_al_2016_MolEcol_Dryad

A maximum clade credibility (MCC) phylogenetic species tree in Nexus format constructed using *BEAST 1.8.1 based on the alignment included in this data package

Hypogymnia recurva and Hypogymnia wilfiana spp. nov., two new lichens from western North America

Hypogymnia metaphysodes was first described from Japan and Sakhalin, and later reported from western North America. Here we show that the North American material currently referred to H. metaphysodes differs from that species not only morphologically an

Sticta torii sp. nov., a remarkable lichen of high conservation priority from northwestern North America

peer reviewedSticta torii Simon & Goward sp. nov. is an isidiate lichen on Alnus, Malus and Picea branches in hypermaritime regions of northwestern North America. It is a rare species, currently known from only a few localities along a narrow longitudinal range in Southeast Alaska, British Columbia and Oregon. It differs from S. fuliginosa and S. sylvatica in its smaller, more irregular lobes and generally well-developed fringe of marginal isidia, and from S. beauvoisii in its smaller size, less elongate lobes and distinctly arbuscular to penicillate marginal isidia. Also diagnostic are the cyphellae, the basal portions of which bear cells with numerous papillae – a feature shared with a small group of closely allied neotropical species including the recently described S. arbuscula and S. arbusculotomentosa. These latter species, however, bear tomentum over the upper surface, unlike S. torii, which is glabrous